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Research Journal of Pharmacognosy 5(3), 2018: 79-97 Received: 7 Sep 2017 Accepted: 16 Jan 2018 Published online: 23 June 2018 DOI: 10.22127/rjp.2018.64880 Review article

Ethnobotanical Applications and Their Correspondence with Phylogeny in -Apioideae

Seyed Hamed Moazzami Farida1, Abdolbaset Ghorbani 2,3*, Yousef Ajani4, Mohammad Sadr5, Valiollah Mozaffarian6

1Department of Biology, Faculty of Science, Bu-Ali Sina University, Hamadan, . 2Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Sweden. 3Traditional Medicine & Materia Medica Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 4Plant Bank, Iranian Biological Resource Center (IBRC), Karaj, Iran. 5History of Science, Encyclopedia Islamica Research Center, Tehran, Iran. 6Research Institute of Forests and Rangelands, Tehran, Iran.

Abstract The Apiaceae family includes some of the most known medicinal, food and in the world some of which have been used by humans since antiquity. Local people in different regions use many species of the family but the information regarding their uses is scattered. Traditionally used species are good candidates for bioprospecting. Combining traditional uses with phylogenetic data helps in selecting species for bioprospecting. In the present study, an ethnobotanical literature review was conducted to outline a comprehensive overview of the ethnobotanical importance of the family in Iran. To highlight the most ethnobotanically used groups in the family, ethnobotanical data were overlapped with generic phylogeny tree of the subfamily Apioideae. In total, 72 species (17.27%) from 42 genera (33.87%) were found to have ethnobotanical uses. Main uses of the family members were medicinal purposes (67.30%) followed by culinary (25%) and ethnoveterinary (11.11%) uses. Two categories of potential species groups for further bioprospecting investigations have been identified based on the phylogenetic analysis. Based on the findings of the present study, phylogenetic analysis can help in identifying potential groups for bioprospecting studies. More rigorous phylogenetic analysis that combines chemotaxonomy data, ethnomedicinal data and phylogenetic data are necessary to pinpoint exact lineages for specific medicinal properties.

Keywords: Apiaceae, ethnobotany, L., Iran, medicinal uses, phylogeny Citation: Moazzami Farida SH, Ghorbani A, Ajani Y, Sadr M, Mozaffarian V. Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae. Res J Pharmacogn. 2018; 5(3): 79-97.

Introduction The Apiaceae family (Umbelliferae) is one of the asafetida (Ferula assa-foetida L.), largest families in the world including more (Cuminum cyminum L.), (Pimpinella than 455 genera and 3600-3780 species [1-3]. anisum L.), (Coriandrum sativum L.), Members of the family are widely distributed (Petroselinum crispum (Mill.) Fuss), and almost all over the world from temperate to (Daucus carrota L.), some of them have subtropical and tropical regions. The family been used by humans since ancient times [4]. includes some important aromatic and medicinal Many species are used in traditional and folk and culinary and such as medicine throughout the world [5] and many root (Foeniculum vulgare Mill.), female have therapeutic values because of rich bioactive ginseng ( sinensis (Oliv.) Diels), compounds such as terpenoids, coumarins,

*Corresponding author: [email protected] © 2018. Open access. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/) Moazzami Farida S.H. et al. sesquiterpenes, flavonols, essential oil Apiaceae family in Iran and to facilitate and components as β-phellandrene and α-terpineol guide future bioprospecting research on the and fatty acids like petroselinic acid [6-9]. members of this family. Iran is a major diversity center of Apiaceae among Asian countries [10-11]. The family is Methods represented by 124 genera and 417 species, An extensive literature review with a focus on distributed in different parts of the country, while ethnobotany and traditional uses of Apiaceae in 114 species are endemic [12-13]. Some large Iran was conducted. Publications in Persian and genera like Ferula L. (34 spp.) and Dorema D. English languages were assessed. Literature Don. (7 spp.) are distributed mainly in Irano- without taxonomic data or with doubtful Turnian region. They include several important identifications or without proper voucher economic and medicinal species like specimen documentation was excluded from the (F. assa-foetida L.), (F. gummosa analysis. All information regarding different uses Bioss.), sagapenum (F. persica Willd.), and of Apiaceae species, scientific and vernacular (Dorema ammoniacum D. Don) names, their uses, used parts, modes of that are distributed mainly in central and southern preparation and administration and geographical parts of Iran [14-16]. Gum ammoniac, gum locations were extracted and tabulated in an excel galbanum and gum asafoteida are among the spreadsheet. Each specific use reported in the important Apiaceae exudates products exported literature for a given species was considered as from Iran [17]. There are many other species that one use report for that species (Species-use are used in different parts of Iran. However, reports). Ethnobotanical uses were categorized accounts on their ethnobotanical uses are into three main groups: medicinal uses, culinary scattered in local reports or other publications uses including vegetables and spices and and there is a need for an inclusive review that ethnoveterinary uses. Furthermore, medicinal gives an overview on the ethnobotanical uses were organized into 20 use categories [21- importance of the family in the region. 22]. Inferential statistical analysis were It has been shown that when traditional plant uses conducted using excel software. Information of a group of taxa are mapped over phylogenetic about the ethnobotanical uses of Apiaceae lineages of that group, evolutionary patterns of species was compiled from 56 sources, including distribution of useful plants in some lineages are published articles and two books. Botanical revealed [18-19]. This suggests that phylogenies nomenclatures were verified using Flora Iranica can be used as tools for identifying potential [23], Flora of Iran [15] and [24]. useful plant lineages and to target investigations All literature sources have been given in table 1. to groups with the highest potential of bioactive For phylogenetic analysis, medicinal and culinary compounds [20]. Combining an ethnobotanical uses of species were overlapped on a generic approach together with phylogenetic analyses level phylogenetic tree [3]. Percentage of useful seems to be a promising methodology for finding species for each was calculated and lineages with desired chemical or medicinal highlighted on the tree. properties [18-19]. The present review has aimed to compile and Results and Discussion collate a database of ethnobotanical uses of Diversity of useful species Iranian Apiaceae and has presented a Ethnobotanical uses were grouped into three comprehensive account of different main categories including medicinal, culinary ethnobotanical use of the family. Further, (including vegetables and spices) and veterinary ethnobotanical uses have been mapped over the uses. A total of 72 species (17.27% of total generic phylogenetic tree of the family to species of the family) from 42 (33.87%) genera understand and interpret the patterns of use were found to be used at least in one of the main distribution over phylogenetic lineages and categories. Main uses of the family members investigate these patterns for making predictions were medicinal purposes (67.31%) followed by on potential species and genera for further culinary (25%) and ethnoveterinary (11.11%) pharmacological studies. This review has tried to uses. Table 1 gives details of the species and highlight the ethnobotanical importance of theirs uses along with the corresponding 80 Res J Pharmacogn 5(3), 2018: 79-97

Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae references. The genera of Ferula (14 spp.), In terms of ethnomedicinal uses, Ferula assa- and Prangos (4 spp.) and Carum, and foetida L. is a very valuable species in traditional (3 spp.) included the highest number medicine and showed the maximum number of of useful species. Ferula is the largest genus of use reports (61 use reports), followed by Apiaceae in Iran and also one of the most Foeniculum vulgar (60 use-reports), Anethum economically exploited genera [12]. graveolens L. (56 use reports) and Coriandrum sativum (49 use reports). The wider utilization of Plant part used these species might relate to the presence of Depending on the use category, different plant effective bioactive constituents. Also, the parts of the Apiaceae were used most. mentioned species were the most popular plants Considering all types of uses together, the most reported for a majority of the medicinal and non- frequently used parts were seeds (26%) followed medicinal uses. by (19%) aerial parts (11%) and roots Although, Apiaceae species are mainly used for (10%) (figure 1). Both seeds and leaves were digestive system afflictions but they have most favored parts in many reports likely because applications for genitourinary health problems, they contain high concentration of bioactive infections/infestations, and respiratory compounds [25] and they are easily available. It conditions. is also thought that the leaves contain more easily According to the reviewed references, 52 species extractable phytochemicals, crude drugs and were recorded as being used for digestive system many other mixtures that may be regarded as disorders. Foeniculum vulgar, Bunium persicum valuable in phytotherapy [26]. However, in (Boiss.) B. Fedtsch., Anethum graveolens, medicinal and culinary applications, the seeds Heracleum persicum Desf. ex Fisch., C.A.Mey. & Avé-Lall., Ferula were the most frequently used plant part (25% assa-foetida, Coriandrum sativum and Cuminum and 50%, respectively) and gum and aerial parts cyminum were used to treat a wide variety of were the most frequently used parts (25%) in the digestive disorders such as gastritis and showed ethnoveterinary category. to have carminative and digestive effects. A total

of 29 species have been documented as being Modes of preparation and administration used for genitourinary system disorders (figure Decoction was the most common way of 3). Foeniculum vulgare, Anethum graveolens, preparation of medicines (36.11%), followed by and Petroselinum crispum were mostly used as infusion (21%) and grinding plant parts (15.28%) diuretic and to stimulate menstruation in young (figure 2).Water was frequently used as the women, and were used for reducing and relieving solvent if required. menstrual pain. The infections/infestations were the third Medicinal uses frequent category of ailments for the studied Medicinal use reports have been categorized into family. Thirty-nine species were used for treating 20 health system disorders [21-22]. A total of 752 infectious diseases; the most common was Ferula use records have been documented. Members of assa-foetida. Twenty-seven species have been Apiaceae were mainly used for digestive system reported for the treatment of respiratory system disorders (34.6%, 52 spp), genitourinary system ailments including asthma and cough, bronchitis disorders (12.7%, 28 spp), infections/infestations and as expectorant. The effect of Ferula assa- (12.4%, 36 spp) and respiratory system disorders foetida against flu may support the similar reports (8.8%, 25 spp) but they also had wide from traditional manuscripts [60]. applications for muscular-skeletal and nutritional disorders. Sensory system disorders, metabolic Culinary uses and poison remedies were the least common. The According to the European Spice Association, unspecified medical disorders category had the culinary herbs are the edible plants that are lowest number of records (0.1%) (figure 3). Most traditionally added to foodstuff for their natural mentioned medicinal properties were carminative flavorings, aroma, visual appearance and (94 citations), diuretic (44), gastritis treatment preservative purposes [80]. In our analysis, we (35) and vermifuge (29). included plants used as vegetables, spices, and flavorings under culinary use category. 81

Moazzami Farida S.H. et al.

Whole part Aerial parts 4% 11% Stem 2% 9% Gum 8%

Inflorescence 4% Seed 26% Latex 5%

Leaves 19% Root 10% Rhizome 1% 1%

Figure 1. Proportion of different plant parts used for the ethnobotanical purpose in the Apiaceae family

40

30

20

% Species

10

0

Pill Oil Raw Vapor Pickle Powder Infusion Poultice Decoction Extraction Demulcent Fresh paste Tooth brush

Eaten with rice Fresh vegetable Soaked in water Hydrodistillation Additive to foods Modes of Preparation

Figure 2. Mode of utilization of the Apiaceae plants

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Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae

Figure 3. Percentage of species and citations in each medicinal use category

Apiaceae family included many species that have rural people use local herbal medicines for the been used as flavoring agents, and treatment of their domestic animals and the role spices in food products since the ancient times of ethnoveterinary medicine in livestock due to their pleasant aroma and also as development is beyond dispute [81]. In spite of preservatives. Among 72 plants reported in this the importance of ethnoveterinary applications of review, 23 species were mentioned to have medicinal plants for rural communities, few culinary applications. From the reported species, studies have been conducted on ethnoveterinary 44% were used as flavourings, 22% as fresh uses of plants in Iran. Only nine species of vegetables, 17% as condiments and 11% as Apiaceae were documented for application in spices (figure 4). Bunium persicum, Coriandrum primary health care of ruminants and treatments sativum and Heracleum persicum were the most of different ailments in animals. Cuminum frequently used culinary plants of Apiaceae in cyminum, Dorema ammoniacum, and Oliveria Iran. decumbens Vent. were reported as the prevailing species, which were used for ethnoveterinary Ethnoveterinary uses purposes. The routine maladies of livestock were In a broad sense, ‘ethnoveterinary medicine’ is diarrhea, infections/infestations, nutritional the science that specifically deals with treating disorders, digestive disorders, and pustules that ailments of livestock and other domestic animals were treated with these medicinal plants (figure with herbal medicine, which plays a key role as 5). The usages of two species of Dorema for the major source of medicine being used to cure infectious wounds have been also documented. animals in rural area [81-82]. A large number of 83

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Table 1. List of medicinal plants of Apiaceae and details of their uses Parts Preparation / Scientific name Local name Uses References used Administration As carminative, to ease digestion, as diuretic; for Alaf-e osghofi, dyspepsia, gastritis, kidney Decoction, Ammi majus L. amy, khalal Ap, Se [5,12,27-29] stones, psoriasis and skin powder/Oral dandan allergies, as tooth stick and general tonic To relieve abdominal pain, back pain, low back pain and joint pain. For bladder inflammation, and nephritis (kidney inflammation), as diuretic. For amenorrhea (missed period), menstrual cramps, dysmenorrheal problems and Mitkham, shabat, impotence. It can cause abortion. Decoction, Anethum graveolens Ap, F, Le, shevet, shevid, As appetizer, to ease digestion, infusion, powder, [28,30-46] L. Se toragh against bloating, nausea, raw / Oral gastritis, gastric reflex in children, hyperchlosterolemia, hyperlipidemia; to reduce blood sugar, hypertension, to increase lactation in nursing mothers; anti- seizure and sedative, helps dyspnea, hiccup and common cold; culinary uses To relieve asthma, headache and low back pain;aAs carminative, diuretic, sedative and general Decoction, Apium graveolens L. Karafs Le, Se tonic. For rheumatic diseases, to vapor/Oral, [12,30-34,38,47] stimulate menstruation inhalation (amenorrhea) and urinary tract infection; culinary uses Apium nodiflorum For chronic skin disorders and as NA Le NA [5] (L.) Lag. diuretic Bunium cylindricum (Boiss. & Hohen.) Zireh-e siyah Se As carminative NA [34] Drude As appetizer, carminative, astringent, decongestant, diuretic, spasmolytic, sedative. Gharah zireh, For children earache, cough; to zireh, zireh-e- Hydrodistillation, Bunium persicum Ap, Le, ease digestion, as stomach tonic, [12,29,33-34,37- Irani (Kermani), decoction, (Boiss.) B.Fedtsch Se, St to help indigestion and vomiting, 39,41-42,48] zireh-e kuhi, powder/Oral gastritis; to increase lactation in zireh-e siyah nursing mothers and against infection; helps weight loss; culinary uses Decoction, Buplereum falcatum To relieve fever, joint pains and NA Le, Se poultice/Oral, [49] L. for wound healing topical Bunium Zireh-e siyah-e- Se As carminative; culinary uses NA [32] bulbocastanum L. kermani To relieve asthma, Hoshtarak, zireh, hyperlipidemia, impotence and zireh-e siyah, parasite infections; to increase Decoction, Carum carvi L. Le, Se [12,31,40,50,51] zireh-e siyah-e lactation in nursing mothers; as infusion/Oral europaei carminative, diuretic and to ease digestion. Culinary uses. 84 Res J Pharmacogn 5(3), 2018: 79-97

Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae Table 1. Continued Parts Preparation / Scientific name Local name Uses References used Administration As blood thinner, carminative for children, vermifuge; against Carum copticum (L.) Decoction, Ezbootk, zeniyan Se cholera, fever, cough, [32,51] C. B. Clarke powder/Oral dysmenorrheal, gastritis and hyperlipidemia Chaerophyllum Chelghaba, St Culinary uses Eaten with rice [52] macropodum Boiss. garkava Chaerophyllum sp. Ghurdumana Se As carminative NA [32] Against cholera and skin Conium maculatum Bikh-e shokaran R, Se allergies; for hair removal and as NA [32,34] L. sedative Against seizure, diabetes, acne; to relieve dental pain, headache, general pain, sore throat and as sedative; used as aphrodisiac, Decoction, appetizer, carminative, stomach [27,30-36,39, Coriandrum sativum Gardilu, geshnij, Ap, Le, extraction, tonic, vermifuge and diuretic; to 41,43,44,46, L. geshniz Se, St infusion, powder, increase lactation in nursing 48,53-54] raw vegetable/Oral mothers, against hyperlipidemia, gastritis, gastrointestinal infections, gout and jaundice; culinary uses To relieve abdominal pain, body pains, colic pain, post-delivery pains, menstrual pain, gastric reflex, gastritis, asthma and dyspnea; used as carminative, stomach tonic, spasmolytic, diuretic, blood tonic, for diarrhea, for healing fractures, to Decoction, Cuminum cyminum increase lactation in nursing infusion, poultice, [31-32,34,37-38, Zireh-e sabz Le, Se L. mothers, for bloating and powder/Oral, 40,42,55-56] inflammatory bowel disease, topical against parasite infection and to stimulate menstruation (amenorrhea) in young women; it helps weight loss; culinary sues. Ethnovetrinary use: as aphrodisiac for camel and carminative for cattle and sheep As appetizer, laxative, diuretic, stimulant, for constipation; to Daucus carota L. Gezar, havij R, Se improve eyesight, to stimulate NA [32-34,42-43,58] menstruation (amenorrhea) and for anemia; culinary uses Against acne, bronchitis, asthma, infection and intestinal parasites. To relieve bladder inflammation, colic pain, sciatic pain, cough, gastritis and seizure. As Dorema Ashtarak, kandal, expectorant, laxative, stimulant, Gu, La, R, [32-34,39,49, ammoniacum D. koma, oshgh, to ease digestion, to heal wounds Pill/Oral Re 56,59-61] Don. oshtorak, vasha and pustules and to stimulate menstruation (amenorrhea). It can cause abortion. ethnovetrinary uses: healing infectious wounds and pustules in animals Against asthma, bronchitis and Ashtarak, balhar, as expectorant; to cure burnings Ap, Gu, bilhar, kal, and constipation; culinary uses. Fresh paste/Oral, [12,39,49,52,54,5 La, Le, R, Boiss. kandal-e kuhi, Ethnovetrinary uses: for gastritis, topical 6] St koma, zou, zu parasite infection and wound healing.

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Moazzami Farida S.H. et al. Table 1. Continued Parts Preparation / Scientific name Local name Uses References used Administration To relieve low back pain, Baghiz, cheshm-e Ducrosia anethifolia Ap, In, delivery pain and irregular Decoction, baghiz, maial, [36,38-39,48,62] (DC.) Boiss. Wp menstruation; as carminative and raw/Oral moshgak, rashgak against gastritis and infection Ducrosia assadii Baghiz, maial, As carminative and vermifuge Decoction, soaked Se [28,49] Alava moshgak bakraii and against gastritis in water/Oral For common cold, cough, fungal Decoction, Echinophora Keravi, Ap, Le, infection and kidney stones; extraction, [46,53,62-65] platyloba DC. khosharizeh Wp culinary uses infusion/Oral As carminative, expectorant, Eryngium Ap, Le, R, sedative and spasmolytic; against billardierei Heldr. Chichagh, zul Decoction/Oral [38,48,52,65] St constipation, fungal infection, ex Boiss. pertussis and rheumatic diseases Eryngium bungei Shochagh Ap As sedative NA [48] Boiss. Eryngium caeruleum Chuchagh, zalang Le Culinary uses NA [12] M.B. Eryngium campestre As appetizer and carminative; Decoction, fresh Zallash F, St [66] L. against kidney stones. vegetable/Orally Eryngium Sisak teli, zulnak Le Culinary uses Oral [67] caucasicum Trautv. As carminative and hemostatic; Decoction, powder, against cough, fever, gastritis, [12,34,38,45, Falcaria vulgaris Ghaz yaghi, Ap, Le, fresh hypertension, stomach problems, 46,53- Bernh. paghaze Se, St vegetable/Oral, vitiligo, and for wound healing; 54,61,68,69] topical culinary uses As carminative and to ease Ferula alliacea digestion; against seizure, Barijeh Gu NA [5,12] Boiss. intestinal infection and parasites and to cure scorpion stings Ferula angulata As carminative and against Chavir, chenour Gu, Le NA [38,52,70] (Schltdl.) Boiss. infection; culinary uses Used as aphrodisiac, diaphoretic, sedative, spasmolytic, expectorant, laxative, and carminative; against intestinal parasites, seizure, ascites, asthma, bronchitis, cholera, Anghuzeh, common cold, cough, Extracted in Gu, La, [12,33,38-39,42, Ferula assa-foetida anghuzeh-e constipation, and diabetes; to vinegar or oil, Le, R, Re, 51-52,59-60,71- L. hangoo, gane-bu, ease digestion to relieve pain, powder/Oral, St 73] heltit, peterk tremor, dyspepsia, earache, topical fever, gastritis, gastric ulcer, hemorrhoid, hiccup, hypertension; as insect repellent, liver tonic, to cure tooth cavity and wounds. It can cause abortion. Ferula behboudiana Against infection; ethnovetrinary (Rech.f. & Esfand.) Anio, kame F, In, Le Decoction/Oral [70] uses: appetizer for cattle Chamberlain To relieve colic pain, earache and infection; as insect repellent, Ferula foetida to remove parasite infection, to Anghuzeh Gu, R Powder/Oral [29,34] (Bunge) Regel stimulate menstruation (amenorrhea), and for wound healing Ferula galbaniflua Barijeh Gu For gastritis and wound healing Poultice/Topical [32] Boiss. & Buhse. To relieve asthma, hiccup, Ferula galbanum L. Anghuzeh La parasite infection, gastritis, and Infusion, pill/Oral [30] as carminative

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Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae Table 1. Continued Parts Preparation / Scientific name Local name Uses References used Administration As appetizer, stomach tonic and vermifuge; to cure common cold, Angiyun, barijeh, Gu, R, Se, dust allergy, dyspepsia, stomach NA [33-34,52-53] Boiss. ghasni St problems, liver cists, wounds and to stimulate menstruation (in amenorrhea) Ferula haussknechtii Komeh, komieh In, Le For infections NA [70] Wolff ex Rech.f. Ferula Hydrodistillation/O hezarlalehzarica Y. Kahoo vahshi Rh, St As carminative and for gastritis [49] ral Ajani To ease digestion and for Ferula latisecta Sasekoma Ap, Le gastritis in children, also as NA [53,74] Rech.f. & Aell. vermifuge To relieve asthma, cough, dental Ferula oopoda Ejek-ghamaghi, Demulcent, pill, pain, headache (migraine), tooth (Boiss. & Buhse.) kal, kal ja-shour, Gu, La, Se vapor/Oral, topical, [30,38-39,48,75] infection and as diuretic, Boiss. koma-e ghalafdar inhalation expectorant, spasmolytic F, Re, Se, To relieve constipation and Ferula ovina Boiss. Koma Decoction/Oral [58,62,65,72] St infection For bites, low back pain, Ferula persica Anghuzeh, Gu, La rheumatic diseases, cough and as Poultice/Topical [32,48,59] Willd. sakbinaj laxative and spasmolytic To relieve asthma and hiccup Ferula sp. Anghuzeh La Infusion/Orally [50] and as carminative. Anghuzeh-e To relieve asthma, cough, Demulcent, pill, Ferula szowitziana shirin, ghamagh- Gu, La, R rheumatic diseases, skin wounds vapor/Oral, [5,30,42] DC. mumi, sagapen and as stomach tonic external, inhalation Ferulago angulata Poultice, Chenour, garchik Ap, La For wound healing; culinary uses [49,54] (Schlecht.) Boiss. powder/Oral To relieve abdominal pain, back pain, joint pain, low back pain, colic pain, dental pain, menstrual pain, post delivery pains, cough, Badian, badian-e asthma, bronchitis, diarrhea, sabz, badio, gastritis and reflex; as appetizer, Decoction, Ap, F, La, Foeniculum vulgare badioun, carminative, sedative, diuretic, hydrodistillation, [27,30-37,39-43, Le, R, Se, Mill. raajuneh, raz, digestive; to remove gallstones infusion, 46,51-52,55,61] St razianeh, and urinary tract stones, to cure powder/Oral zaljooneh gout, hemorrhoid, bloating, kidney infections and parasitic infection; to increase lactation in nursing mothers and to stimulate menstruation (in amenorrhea). Froriepia subpinnata (Ledeb.) Chuchugh, zalang Se Culinary uses NA [12] Baill. Haussknechtia To relieve diabetes and decoction, fresh Kelos-e kuhi Ap [44,52,76] elymaitica Boiss. hypertension vegetable/Oral Heracleum Jengel-e Se To ease digestion; culinary uses Additive to foods [30] gorganicum Rech. f. ghamaghi Heracleum Golpar, kereson Se Against infection; culinary uses NA [62] lasiopetalum Boiss. As appetizer, carminative, stomach tonic, vermifuge diuretic and sedative; to relieve Decoction, Kolek, koolak, [5,12,32- Heracleum persicum F, Le, R, dyspepsia, gastritis in children, infusion, koolakpar, 34,40,67, 75,77- Desf. Se headache (migraine), hiccup, flu, pickle/Oral, food golpar, golspar 79] infection and skin diseases; also flavoring used to ease digestion and as mouthwash; culinary uses For cleansing blood and healing Hydrocotyl vulgaris Ab boshghabi-e Wp wounds and as diuretic and NA [64] L. mamuli laxative

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Moazzami Farida S.H. et al. Table 1. Continued Parts Preparation / Scientific name Local name Uses References used Administration Kelussia To relieve cough, rheumatic Bakhtyari karafs, odoratissima Le, Wp diseases, diabetes and dyspepsia; NA [12,44,61-62] keluss Mozaff. culinary uses Lagoecia Alaf-e kaaji, Ap For diarrhea and gall stones Infusion, raw/Oral [29,36,52] cuminoides L. zireh-e vahshi Laser trilobum (L.) As carminative; ethnovetrinary NA Le, Se NA [5] Borkh. use To relieve asthma, diabetes and gastritis; as carminative, diaphoretic, diuretic, sedative, Levisticum officinale stimulant and heart tonic; to ease Infusion/Oral, Karafs-e kuhi Le, R, Se [5,34,39,44,49] W. D. J. Koch. digestion, to induce sweating, to eaten as vegetable stimulate menstruation (amenorrhea) and to cure nervous disorders; culinary uses To relieve thirst in children, dyspepsia, gastritis, Den, denak, la’le Oliveria decumbens AP, In, gastrointestinal disorders and Decoction/Oral, biaban, nuneh [27-28,52,60,63] Vent. Le, Se infection and as carminative; eaten as vegetable khoda ethnovetrinary use: to cure diarrhea in sheep and goats Opopanax hispidus Alaf shir In, Le, St Against infection. NA [70] (Friv.) Griseb. As aphrodisiac, appetizer, carminative, expectorant, diuretic, spasmolytic and general tonic; to relieve low back pain, Jafari, tokhm-e joint pain, menstrual pain, fever, Petroselinum kalam Ap, Le, R, diabetes, bladder disorders, Infusion, oil/Oral, [31-34,38,41- crispum (Mill.) Fuss (Parsley=Eng. Se, Wp dysuria, fatigue, gout, kidney topical 42,44,59]

Name) problems and kidney stone; to increase lactation in nursing mothers and to stimulate menstruation (amenorrhea); culinary uses To relieve cough, kidney stones, Peucedanum Not Bokhur ol ekrad meningitis, respiratory ulcers and NA [60] officinale L. available as diuretic To relieve colic pain, bloating, common cold, cough headache (migraine), menstrual pain, Anison (badian Decoction, Pimpinella anisum gastritis, gastric reflex, nausea roomi), anisun, Le, Se hydrodistillation, [32-34,40,51,70] L. and infection; as diuretic, raz, vaveh shing infusion / Orally carminative, vermifuge and to increase lactation in nursing mothers; culinary uses Prangos acaulis As appetizer and against parasite Jashir-e kutooleh Gu, St NA [64] (DC.) Bornm infection; culinary uses Prangos cheilanthifolia Sakbinaj Ap As carminative NA [48] Boiss. As carminative, diuretic, laxative and sedative; to relieve pain, Bale har, ginu, Prangos ferulacea Ap, F, Le, dyspepsia, parasite infection and javsheer, jhashir, Decoction/Orally [43,60,62-63,70] (L.) Lindl. Se, Sh vomiting; it can cause abortion; jooshir, marzah ethnovetrinary use: to remove lice and ticks in animals Prangos uloptera Jashir-e sakhreh As carminative, against infection F, Le NA [62,72] Dc. roui, kharkool and tonic Psammogeton canescens (DC.) Shen jar F, Le Against infection; culinary uses NA [72] Vatke

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Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae Table 1. Continued Parts Preparation / Scientific name Local name Uses References used Administration To relieve muscle pain, bad Pycnocycla Decoction, breath, to cure snake scorpion aucherana Decne. Sak dandan Le, R poultice, tooth [29,51] and insect bites and to remove Ex Boiss. brush/Oral urinary tract stones Sanicula europaea Not As stomach tonic and for wound Marhami NA [79] L. available healing Scandix pecten- For blood coagulation, body Suzanak Ap Decoction/Oral [53] veneris L. pains and palpitation Scandix stellata Badian-e kuhi Wp As stomach tonic NA [48] Banks & Soland To relieve hypertension, parasite infection, prostate problems, Smyrnium Andol, avandol, urinary tract diseases and Decoction, Ap, R, Se [45,52,60] cordifolium Boiss. gonour, ovandol gynaeco-urinary disease; infusion/Oral ethnovetrinary use: urinary retention in horse and mule Thapsia garganica Not To reduce appetite, as Safsia NA [60] L. available carminative and nerves tonic Trachydium Shaghaghi R To improve memory NA [32] lehmanni Benth. To relieve colic pain, common cold, gastric reflex, gastritis and Ajghu, keserk, Hydrodistillation, Trachyspermum nausea; as carminative and zenian, zenyan F, R, Se decoction, [33-35,37,42,55] ammi (L.) Sprague vermifuge and to increase (khordaneh) raw/Oral lactation in nursing mothers; culinary uses Turgenia latifolia Dareh jouyi Ap For urinary tract problems Infusion/Oral [52] Hoffm. Zosima orientalis For digestive and nerve system Karafs-e kuhi Se NA [34] Hoffm. disorders Se: seed, Le: , R: root, Ap: aerial part, St: stem, Gu: gum, La: latex, Wp: whole part, In: inflorescence, F: flower, Re: resin and Rh: rhizome. NA: not available

Generally, freshly collected plants or plant parts clade might have similar medicinal properties as were used for treatment. Most commonly used their relatives. As a result, it points out the plant parts were gum, aerial parts, seeds, and species or genera with potential bioactivity for stems. Some of the commonly used future research on drug discovery and ethnoveterinary medicines were the decoction of bioprospecting. Some clustering of medicinal the leaves and of Ferula behboudiana as species could be seen on the tree in figure 6. appetizer while aerial parts of Oliveria Based on this figure, the potential medicinal decumbens, Prangos ferulacea (L.) Lindl. and plants for future bioprospecting could be grouped Smyrnium cordifolium Boiss. were used for into two categories. The first category was treatment of diarrhea, lice, and ticks in sheep and species without any use record in genera that goats and urinary retention in horse and mule, already contained useful species. For example, respectively. the genus Eryngium included 12 species in total, from which three already used medicinally and 2 Phylogenetic pattern of ethnobotanical uses culinary. The other seven members of this genus Medicinal and culinary uses were overlapped on that do not have any use reports might have a genus level phylogenetic tree in Apiaceae- similar properties and bioactive compounds as Apioideae [3]. Clusters of genera with medicinal their relative species in the genus. The species of uses have been shown in figure 6. This figure has the first category included plants in genera shown potential groups of plants having Eryngium, Buplerum, Anthriscus, Scandix, medicinal properties based on the phylogenetic Daucus, Dorema, Ferula, Heracleum, Zosima, relation with known medicinal species. The Ducrosia, Peucedanum, Bunium, Pimpinella, rationale behind is that if a clade contained a Psammogeton, Opopanax, Pycnocycla, number of medicinal species or genera, then it is Echinophora, Bifora, Carum, Falcaria, and very likely that other species or genera in that Prangos (figure 6). The second category included

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Moazzami Farida S.H. et al. species in the genera where their sister groups in Tetrataenium, Tordylium, Trigonosciadium, the same clade contained medicinal species. For Kalakia, Cymbocarpum, Elaeostica, Galagania, example in the tribe Ferulinae, both Ferula and Hyalolaena, Muretia, Aphanopleura, Dorema contained medicinal species. Damavendia, Opsicarpium, Zeravschania, Therefore there was a big chance that species of Smyrniopsis, Anisosciadium, Dicyclophora, Leutea possessed similar properties and bioactive Chamaesciadium. Fuernrohria, compounds (figure 6). The second category Gongylosciadium, Grammoscadium, includes Hohenackeria, Lecokia, Chaerophyllum, Rhabdosciadium, Alococarpum, Azilia, Leutea, Athamanta, Laserpitium, Orlaya, Bilacunaria, Diplotaenia and Eriocycla. Polylophium, Malabalia, Pistinaca, Semenovia,

Figure 4. Proportion of different applications for culinary purpose in the Apiaceae family

Figure 5. Percentage of ethnoveterinary use category

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Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae

Figure 6. Distribution of medicinal species and their ration to the total number of species in each genus along the generic phylogenetic tree

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Figure 7. Distribution of culinary species and their ration to the total number of species in each genus along the generic phylogenetic tree

In some clades, the phylogenetic signal was very have shown that there is a phylogenetic clustering weak (Selineae, Cachrys clade, Torilidinae, pattern of plants with medicinal properties across Pleurospermeae) and only few members had different plant groups [18, 83-84]. medicinal uses but in some other clades such as Distribution of edible and culinary species along Apieae, this signal seemed strong with many the phylogenetic tree seemed different from members being medicinally used. Other studies medicinal species (figure 7). Although the family

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Ethnobotanical applications and their correspondence with phylogeny in Apiaceae-Apioideae includes some of the oldest known edible species, [5] French DH. Ethnobotany of the Umbelliferae. they were distributed within few certain groups The biology and chemistry of the including Apieae, Careae, Coriandreae, Umbelliferae. London: Linnean Society, Sinodielsia clade and Daucinae. 1971. [6] Coruh N, Celep AS, Özgökçe F. Antioxidant Conclusion properties of Prangos ferulacea (L.) Lindl., The current study gives an overview on the Chaerophyllum macropodum Boiss. and available ethnobotanical information of Apiaceae Heracleum persicum Desf. from Apiaceae and detailed information on their uses. It show family used as food in Eastern Anatolia and that medicinal and culinary properties are not their inhibitory effects on glutathione-S- randomly distributed across the species in transferase. Food Chem. 2007; 100(3): 1237- Apiaceae and they tend to be present in some 1242. phylogenetic pattern. It highlights the potential [7] Razavi SM, Nazemiyeh H, Hajiboland R, species groups of the family for further Kumarasamy Y, Delazar A, Nahar L, Sarker bioprospecting investigations; however, more SD. Coumarins from the aerial parts of rigorous phylogenetic analysis combining Prangos uloptera (Apiaceae). Rev Bras chemotaxonomy is necessary to pinpoint the Farmacogn. 2008; 18(1): 1-5. exact lineages for specific medicinal application [8] Sharififar F, Yassa N, Mozaffarian V. Bioactivity of major components from the and properties. seeds of Bunium persicum (Boiss.) Fedtch.

Author contributions Pak J Pharm Sci. 2010; 23(3): 300-304. [9] Bencheraiet R, Kherrab H, Kabouche A, Abdolbaset Ghorbani designed the study. Seyed Kabouche Z, Jay M. Flavonols and Hamed Moazzami Farida and Abdolbaset antioxidant activity of Ammi visnaga Ghorbani conducted literature review. Seyed L.(Apiaceae). Rec Nat Prod. 2011; 5(1): 52- Hamed Moazzami Farida, Mohammad Sadr, and 55. Abdolbaset Ghorbani conducted data analysis. [10] Pimenov M, Leonov M. The Asian Yousef Ajani and Valiollah Mozaffarian did the Umbelliferae biodiversity database (ASIUM) taxonomic review and nomenclature checks. with particular reference to South-West Abdolbaset Ghorbani, Seyed Hamed Moazzami Farida, and Yousef Ajani drafted the manuscript. Asian taxa. Turk J Bot. 2004; 28(1-2): 139- 145. Declaration of interest [11] Ajani Y, Ajani A, Cordes JM, Watson MF, The authors declare that there is no conflict of Downie SR. Phylogenetic analysis of nrDNA interest. The authors alone are responsible for the ITS sequences reveals relationships within content of the paper. five groups of Iranian Apiaceae subfamily Apioideae. Taxon. 2008; 57(2): 383-401. References [12] Mozaffarian V. Identification of medicinal [1] Petrova SE. Life forms of Apiaceae in central and aromatic plants of Iran. Tehran: Farhang- Russia. Nord J Bot. 2015; 33(6): 747-753. e-Moaser, 2013. [2] Pimenov MG, Leonov MV. The genera of the [13] Valiejo-Roman C, Terentieva E, Samigullin Umbelliferae: a nomenclator. Kew: Royal T, Pimenov M, Ghahremani-Nejad F, Botanic Gardens, 1993. Mozaffarian V. Molecular data (nrITS- [3] Downie SR, Spalik K, Katz-Downie DS, sequencing) reveal relationships among Reduron JP. Major clades within Apiaceae Iranian endemic taxa of the Umbelliferae. subfamily Apioideae as inferred by Feddes Repert. 2006; 117(5-6): 367-388. phylogenetic analysis of nrDNA ITS [14] Mozaffarian V. Two new species and two sequences. Plant Div Evol. 2010; 128(1-2): new records of Umbellifera from Iran. 111-136. Rostaniha: Syst Biodivers Fungi Plant. 2013; [4] Judd WS, Campbell CS, Kellogg E, Stevens 14(1): 36-42. P, Donoghue M. Plant systematics: a [15] Mozaffarian V. Umbelliferae. Tehran: phylogenetic approach. Sunderland: Sinauer Institute of Forests and Rangelands Press, Associates, 2008. 2007.

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